Plant metabolic responses to soil herbicide residues differ under herbivory in two woodland strawberry genotypes

The use of glyphosate-based herbicides (GBHs) to control weeds has increased exponentially in recent decades, and their residues and degradation products have been found in soils across the globe. GBH residues in soil have been shown to affect plant physiology and specialised metabolite biosynthesis, which, in turn, may impact plant resistance to biotic stressors. In a greenhouse study, we investigated the interactive effects between soil GBH residues and herbivory on the performance, phytohormone concentrations, phenolic compound concentrations and volatile organic compound (VOC) emissions of two woodland strawberry (Fragaria vesca) genotypes, which were classified as herbivore resistant and herbivore susceptible. Plants were subjected to herbivory by strawberry leaf beetle (Galerucella tenella) larvae, and to GBH residues by growing in soil collected from a field site with GBH treatments twice a year over the past eight years. Soil GBH residues reduced the belowground biomass of the susceptible genotype and the aboveground biomass of both woodland strawberry genotypes. Herbivory increased the belowground biomass of the resistant genotype and the root-shoot ratio of both genotypes. At the metabolite level, herbivory induced the emission of several VOCs. Jasmonic acid, abscisic acid and auxin concentrations were induced by herbivory, in contrast to salicylic acid, which was only induced by herbivory in combination with soil GBH residues in the resistant genotype. The concentrations of phenolic compounds were higher in the resistant genotype compared to the susceptible genotype and were induced by soil GBH residues in the resistant genotype. Our results indicate that soil GBH residues can differentially affect plant performance, phytohormone concentrations and phenolic compound concentrations under herbivore attack, in a genotype-dependent manner. Soil GBH altered plant responses to herbivory, which may impact plant resistance traits and species interactions. With ongoing agrochemical pollution, we need to consider plant cultivars with better resistance to polluted soils while maintaining plant resilience under challenging environmental conditions.